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The building was constructed from 1933 to 1937 following plans of architectPaul Ludwig Troost as the Third Reich's first monumental structure of Nazi architecture and as Nazi propaganda. The museum, then called Haus der Deutschen Kunst ("House of German Art"), was opened on 18 July 1937 as a showcase for what the Third Reich regarded as Germany's finest art. The inaugural exhibition was the Große Deutsche Kunstausstellung ("Great German art exhibition"), which was intended as an edifying contrast to the condemned modern art on display in the concurrent Degenerate art exhibition.

On 15 and 16 October 1939, the Große Deutsche Kunstausstellung inside the Haus der Deutschen Kunst was complemented by the monumental Tag der Deutschen Kunst celebration of "2,000 years of Germanic culture" where luxuriously draped floats (one of them carrying a 5 meter tall golden Nazi Reichsadler) and thousands of actors in historical costumes paraded down Prinzregentenstraße for hours in the presence of Adolf Hitler, Hermann Göring, Joseph Goebbels, Heinrich Himmler, Albert Speer, Robert Ley, Reinhard Heydrich, and many other high-ranking Nazis, with minor events taking place in the Englischer Garten nearby. The 1939 Tag der Deutschen Kunst was documented by a group of hobby cinematographers on 16 mm Kodachrome color movie, the resulting 30-minute film is still pristine today due to Kodachrome's unusual archival properties, and is available in a variety of editions on VHS and DVD, such as Farben 1939 - Tag der Deutschen Kunst in München.

After the end of World War II, the museum building was first used by the American occupation forces as an officer's mess; in that time, the building came to be known as the "P1", a shortening of its street address. The building's original purpose can still be seen in such guises as the swastika-motif mosaics in the ceiling panels of its front portico.

Beginning in 1946, the museum rooms, now partitioned into several smaller exhibition areas, started to be used as temporary exhibition space for trade shows and visiting art exhibitions. Some parts of the museum were also used to showcase works from those of Munich's art galleries that had been destroyed during the war. In 2002, the National Collection of Modern and Contemporary Arts moved into the Pinakothek der Moderne. Today, while housing no permanent art exhibition of its own, the museum is still used as a showcase venue for temporary exhibitions and traveling exhibitions, including: Tutankhamun and the Zeit der Staufer and Gilbert and George exhibitions.

Since 1983, the museum building also houses the nightclub, P1, Munich's famous high-society destination.

For approximately 60 million euros the Haus der Kunst is to be redeveloped from 2014. Commissioned for the project is the London-based architect David Chipperfield.